Infection control measures in ophthalmology during the COVID-19 outbreak: A narrative review from an early experience in Italy

Original research article

EJO

Journal of Ophthalmology

Infection control measures in

ophthalmology during the COVID-19

outbreak: A narrative review from

an early experience in Italy

Daniele Veritti

, Valentina Sarao

, Francesco Bandello

and Paolo Lanzetta

Abstract

Introduction: The novel coronavirus (SARS-CoV-2) is infecting people and spreading easily from person-to-person. Cases have been detected in most countries worldwide. Italy is one of the most affected countries as of 30 March 2020. Public health response includes a rapid reorganization of the Italian National Healthcare System in order to reduce transmission of COVID-19 within hospitals and healthcare facilities, while optimizing the assistance to patients with severe COVID-19 complications.

Methods: We analysed the actions that were taken in three ophthalmology centres in northern Italy during the SARS-CoV-2 outbreak and how these measures affected patient’s attendance. In addition, due to the rapidly evolving scenario, we reviewed the evidence available during the course of this pandemic.

Results: A full reorganization of ophthalmology services is mandatory according to current existing infection contain-ment measures in order to continue dispensing urgent procedures without endangering the community with amplifi-cation of the diffusion chain. Ophthalmologists are considered at elevated risk of exposure when caring patients and vice versa, due to their close proximity during eye examination. High volumes of procedures typically generated by oph-thalmologists with concurrent implications on the risk of infection are considered when re-assessing healthcare facilities reorganization.

Conclusion: Containment measures in the event of pandemic due to infective agents should be well known by healthcare professionals and promptly applied in order to mitigate the risk of nosocomial transmission and outbreak.

Keywords

COVID-19, coronavirus, SARS-CoV-2, triage, face mask, personal protective equipment

Date received: 31 March 2020; accepted: 29 April 2020

Introduction

In December 2019, an atypical pneumonia of unknown origin was first reported in a group of patients in Wuhan, China.1 Chinese authorities identified a new betacoronavirus (severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)) as the cause of the out-break.2 SARS-CoV-2 is highly contagious and has evolved into a global health threat within weeks. As of 30 March 2020, the ongoing outbreak of coronavi-rus disease 2019 (COVID-19) originating in Wuhan

1

Department of Medicine – Ophthalmology, University of Udine, Udine, Italy

2

Department of Ophthalmology, Ospedale Santa Maria della Misericordia, Azienda Sanitaria Universitaria Friuli Centrale (ASUFC), Udine, Italy

3

Istituto Europeo di Microchirurgia Oculare (IEMO), Udine, Italy

4

Vita-Salute San Raffaele University, Milan, Italy

5

IRCCS San Raffaele Scientific Institute, Milan, Italy Corresponding author:

Paolo Lanzetta, Department of Medicine – Ophthalmology, University of Udine, P.le Santa Maria della Misericordia 15, 33100 Udine, Italy. Email: paolo.lanzetta@uniud.it

European Journal of Ophthalmology 0(0) 1–8

had caused more than 770,000 confirmed cases and more than 37,000 deaths, with 178 countries/sovereign-ties affected worldwide.3 At the same date, Italy was one of the most affected countries with more than 100,000 confirmed cases and more than 11,000 deaths. Cities like Milan, Bergamo and Brescia, in Lombardy, reported an exponential growth of hospi-talized people infected by SARS-CoV-2. Since 10 March 2020, Italy has been on lockdown. Schools, uni-versities, museums and most shops have been closed and the National Healthcare System is trying to cope with the flood of patients needing hospitalization and intensive care unit support.4The emergence of a novel viral pneumonia constitutes an unprecedented threat and challenge to the community as well as to the healthcare system. Strong hygiene and containment measures and individual citizen responsibility, includ-ing strict self-isolation measures, have been instituted to slow down virus transmission. Also, a rapid infec-tion control response is essential to contain and miti-gate the risk of nosocomial transmission and outbreak. In light of this, since the lockdown, we rapidly modified the organization of our ophthalmology clinics in order to stepping up control measures for SARS-CoV-2 infection. Working modalities are continuously evolv-ing accordevolv-ing to local regulations and available guide-lines. This article aims to share the local experience of three centres in northern Italy (Department of Ophthalmology, University Vita-Salute, IRCCS Ospedale San Raffaele, Milan; Department of Ophthalmology, ASUFC, Udine; and Istituto Europeo di Microchirurgia Oculare (IEMO), Udine) in order to educate ophthalmologists on necessary measures to minimize impact on both healthcare work-ers and patients. Transitional adopted measures are also discussed with respect to recent published data.

Methods

A review of relevant documents through Internet and database search was conducted in relation to SARS-CoV-2. Pertinent evidence was selected in order to implement strategies to avoid virus infection in ophthalmology. We describe the scenario of three oph-thalmology centres in northern Italy during the SARS-CoV-2 outbreak. The Department of Ophthalmology of the University Vita-Salute, IRCCS Ospedale San Raffaele is located in Milan, a city with 1.3 million inhabitants and a dense and extended urban region with a total population of 5 million people which has already been hit hard by the COVID-19 outbreak. The Department of Ophthalmology of ASUFC is located in Udine, a city with 100,000 inhabitants and serves Italy’s north-easternmost region (1.2 million inhabi-tants). In this region, the COVID-19 epidemic curves

are not yet as dramatic as in Milan and Lombardy, with a slower increase rate. IEMO is also located in Udine. It is an ambulatory surgery centre (ASC) focused on providing same-day diagnostic and surgical care, especially for retinal conditions and intravitreal therapies. We analysed the actions that were taken in the above cited centres and how these measures affect-ed patient’s attendance. In addition, due to the rapidly evolving scenario, we reviewed the evidence available during the course of this pandemic.

Observation

COVID-19: the epidemic and the challenges

reorganized. Most of them have special areas for COVID-19 patients. Some hospitals are acting as hubs to collect patients with COVID-19 and related diseases. Most of the outpatient clinics have been shut down and non-urgent visits are postponed to make resources available for the most severe cases. While the situation is evolving rapidly, newer docu-ments and guidelines are available to advice on best practice.

Strategies to prevent transmission in

ophthalmology clinics

We present a real-life scenario on reorganization of clinical activity at our clinics in order to:

1. Prevent nosocomial transmission amplification events.

2. Provide adequate care of patients with non-deferrable ocular conditions.

3. Facilitate the conversion of a routine care hospital to a hub hospital for assisting patients experiencing COVID-19 complications.

Strategies from all the three ophthalmic centres were generally consistent with some differences that will be detailed below and summarized in Table 1.

Minimize chance for exposures. Avoid hospital-related transmission of the virus. Enforce facility policies and practices to minimize exposures to SARS-CoV-2. Implement measures even before patient arrival with the aim of lowering patient attendance. We applied the following actions:

• Suspension of elective clinical services and resched-uling appointments to patients with non-urgent con-ditions. Due to the relevant volume of subjects attending the outpatient service, selected physicians (including residents), nurses and administrative per-sonnel have been dedicated to screen patients’ records and to contact scheduled patients via phone. In routine conditions, 3000 patients at the hospital in Milan, 590 patients at the hospital in Udine and 110 patients at the ASC are typically scheduled for an ophthalmic evaluation or a diag-nostic procedure in 1 week. Within the first week of the outbreak, a reduction in patients’ attendance by 70%–80% was attained in all institutions. Six hun-dred patients in Milan, 113 patients at the Udine hospital and 30 patients in the ASC were seen due to urgent ocular conditions or underwent non-deferrable diagnostic exams.

• As for surgery, cataract interventions and other elec-tive procedures have been postponed. Intravitreal

therapies were maintained to avoid any delay. There are two reasons for not deferring intravitreal injections. Any delay may possibly cause both ana-tomical and functional irreversible worsening. Furthermore, rescheduling high volumes of injec-tions poses challenges on capacity and available slots. Cancellation of elective surgeries allowed to increase the interval between procedures avoiding massive presence of patients at the clinics and hope-fully reducing the risk of infection. Under normal circumstances, 141 patients in Udine and 330 patients in Milan undergo surgical procedures or intravitreal injections per week. Within the first week of the Italian outbreak, after rescheduling, 71 patients at the Udine hospital and 80 in Milan underwent non-deferrable surgical procedures (reti-nal detachment surgery, glaucoma surgery, ocular oncology surgery, trauma) and intravitreal injections.

Scheduled intravitreal injections were mostly main-tained at the ASC. A number of patients planned for intravitreal therapies at the hospital centres cancelled their appointments. This rate was higher in the Milan centre due to the subset of population referring to the San Raffaele Hospital. Those patients are often residents from other Italian regions who experienced major difficulties in travelling during the outbreak and were at high risk of quarantine after their return home. Some patients skipped the appointment because they did not perceive the urgency of the therapy.

Fortunately, the total time spent at the health facil-ities for receiving intravitreal therapies did change after the outbreak and lockdown. At the hospitals and ASC, respectively, the mean total time decreased from 185 to 102 min and from 1 h to 32 min.

judgement and must always take into account individ-ual patient medical and social circumstances.14 • In order to minimize the influx of patients and

care-givers, guidance is given to convert all accesses that do not strictly require a visit of the patient into a phone contact.

Patient triage. It is particularly important to protect individuals at increased risk for adverse outcomes from COVID-19 (e.g. older individuals with comorbid conditions). In order to protect the patients attending the clinic and the healthcare staff, a rapid safe triage and isolation of patients with symptoms of suspected COVID-19 or other respiratory infections (e.g. fever and cough) are mandatory. We implemented the fol-lowing steps:

• A triage station is set up outside the facility to screen patients prior to entering the clinic.

• Physical barriers are installed (e.g. glass or plastic windows) at reception areas to limit close contact between triage personnel and potentially infectious patients.

• Visual alert icon (e.g. signs and posters) at the entrance and in strategic places (e.g. waiting areas and

elevators) is posted to provide patients and healthcare professionals with instructions about hand hygiene, respiratory hygiene and cough etiquette.

• Supplies for respiratory hygiene and cough etiquette, including alcohol-based hand rub with 60%–95% alcohol, tissues and no-touch receptacles for dispos-al, are positioned at entrances, waiting rooms and patient check-ins.

• Access is limited only to patients with non-deferrable ocular conditions. Presence of caregivers, if not strict-ly necessary, is not allowed inside the clinic. When needed, only one accompanying person is permitted. • Triage of patients with respiratory symptoms is

prioritized.

• At the time of check-in, patients are asked about the presence of symptoms of a respiratory infection and history of travel to areas experiencing transmission of COVID-19 or contact with possible COVID-19 cases in the past 14 days.

• Triage personnel wear surgical face masks. These are also provided to patients with symptoms of respiratory infection at check-in. At the ASC, all patients received a face mask and were instructed on how to wear it. The importance of triage is highlighted by all recom-mendations from different scientific communities.14–17

Table 1. Summary of recommendations.

Measures in this study (10 March 2020)

AAO recommendations (29 March 2020) RCOphth recommendations (19 March 2020)

SOI and AIMO recommendations (18–28 March 2020) Minimize chance for exposures

Suspension of elective clinical services Supported Supported Supported Suspension of elective surgical procedures Supported Supported Supported Maintain intravitreal therapies Not mentioned Supported Supported Patient triage

Safe triage and isolation of patients with symptoms of suspected COVID-19 or other respiratory infection

Supported Supported Supported Reduction of droplet generation and infection transmission

Promote cough etiquette and hand hygiene Supported Supported Supported Slit-lamp barriers Supported Supported Supported Avoid speaking during slit-lamp examination Supported Not mentioned Supported Prefer contact tonometry Not mentioned Not mentioned Not mentioned Use of personal protective equipment

Face masks for symptomatic patients Supported Supported Supported Face masks for healthcare personnel assisting

asymptomatic patients

Not routinely required

At discretion Supported Face masks for asymptomatic patients Not routinely

required

At discretion Supported Other measures

Environmental control Supported Supported Supported Staff education Supported Supported Supported Patient education Not mentioned Not mentioned Supported

Reduction of droplet generation and infection transmission. As the model of transmission is mainly by droplets, we introduced the following measures:

• The waiting rooms are kept as empty as possible by increasing the interval time between appointments, and as much as prudent, the visits of the most vul-nerable patients are reduced.

• We identified a separate, well-ventilated space that allows the waiting patients to be separated by 6 or more feet, with easy access to respiratory hygiene supplies.

• Cough etiquette is promoted.

• Hand hygiene by hand sanitizing with alcoholic sol-utions is performed. Soap and water are used if hands are visibly soiled. Meticulous hand hygiene is strongly recommended during the following steps: before and after all patient contact; before and after using a surgical mask and after removing gloves; after having contact with respiratory and lac-rimal secretions and objects/materials in the envi-ronment surrounding the patient.

• We designed and installed disposable slit-lamp plas-tic barriers as they may provide a measure of added protection against droplet transmission.18,19

• Patients and physicians are strongly recommended to avoid speaking during slit-lamp examination. • Non-contact tonometry (NCT) is a potential source

of microaerosol.20 Therefore, it is prudent to sus-pend the use of NCT in outbreak areas. I-Care tonometry or Goldmann applanation tonometry with the use of disposable tips are encouraged to minimize the risk of cross-infection.

An additional preventive action is to reduce time in close contact during examination as illustrated in the key actions by the Royal College of Ophthalmology.15 Use of personal protective equipment. Healthcare person-nel are on the front lines of caring for patients with confirmed or possible infection with COVID-19 and therefore have an increased risk of exposure to this virus. Moreover, it is estimated that a high percentage of healthcare personnel working in outbreak areas are positive for SARS-CoV-2. Eye examinations typically require less than 3-feet face-to-face distance. Therefore, the correct use of personal protective equipment (PPE) is mandatory in order to prevent nosocomial amplifi-cation events in ophthalmology.

Theoretically, gown, gloves, protective mask and goggles or some sort of good eye protection are recom-mended. However, many hospitals in Italy and Europe have reported shortages of PPE, specifically N95 respi-rators and face masks. In this scenario, alternatives are considered, including other classes of face masks.

Special care is taken to ensure that respirators are reserved for situations where respiratory protection is most important, such as during aerosol-generating pro-cedures on suspected or confirmed COVID-19 patients. Physicians and staff wear gloves before touching any patients with conjunctivitis. Attention is paid to train-ing and proper donntrain-ing, dofftrain-ing and disposal of any PPE. A recent systematic review21found that frequent hand washing, barrier measures including gloves and masks and isolation of people with suspected tory tract infection reduce the transmission of respira-tory viruses. Although the protective effect of surgical masks against relevant aerosolized biological hazards is limited, they are still protective to some extent.22–24

visitors. The importance of environmental control is also highlighted by recent recommendations.14–17 Staff education, infection control training and symptom monitoring. All staff undergo infection control training to familiarize with the proper steps of hand hygiene and donning and doffing of PPE. All clinical staff are required to report any symptoms such as fever, chills, myalgia, sore throat, runny nose, cough, vomiting, diarrhoea or pneumonia as well as on their recent travel histories. We schedule daily virtual meetings to allow staff to receive updated instructions, and share information and data without being physically grouped together. We utilize a free multi-platform online service.

Patient education. Considering the multitude of contacts, it is the responsibility of the staff to provide patient education in order to improve social behaviour and disease understanding:

• Educate to social distancing measures, following Government and Health Authorities’ instructions. • Educate patients to proper eye drop administration

technique. Promote self-instillation.

• Educate eyeglass wearers to disinfect spectacles and glasses. Attention is paid at presbyopic patients using reading glasses, as they may be putting them on and off their face multiple times a day. Promote careful and thorough hand washing.

• Educate contact lens users to proper hand washing before and after insertion and removal.

Additional measures to be considered. The following meas-ures are not yet applied to our centres. However, there is a rationale for their adoption in a clinical setting: • At arrival, all patients and their accompanying

per-sons could be screened using infrared thermometers. • Electronic messaging services – such as short mes-saging service (SMS), mesmes-saging apps or chatbots – could be used in order to provide prompt and useful information to patients.

• When physical barriers are not present between patients and the admittance staff, alternative meas-ures are adopted such as social distancing (at least 3– 6 feet), avoidance of any direct and indirect contact.

Discussion

As of 30 March 2020, more than 11,000 subjects have been killed in Italy and 37,000 worldwide by COVID-19, which has had the worst outbreak outside of main-land China.3Unlike the Great War, this battle cannot be fought with traditional arms, as very few are known

about the enemy and how to fight it. The only weapon that we currently have to avoid the collapse of health-care services is to reduce the spread of this novel virus through containment measures to mitigate the risk of nosocomial transmission. It is critically important to implement proactive infection control actions, which must be planned ahead. There is a massive risk of paying a high price for the lack of training, appropriate tools and proper plans.

Ophthalmologists are at elevated risk of exposure when caring patients, because they work in close prox-imity to patients and serve as the first providers to evaluate COVID-19 positive patients with conjunctivi-tis. Ophthalmologists usually visit a high volume of patients over the age of 60 years, putting them at increased risk of developing COVID-19. Providing patients with a face mask, supplying tissues, promoting cough etiquette and recommending hand hygiene and applying decontamination are all important steps. All healthcare personnel should be aware that they may become a major source of contamination in case they do not attain to simple and yet efficacious hygiene rules. Frequent information and feedback sessions, complemented by clear, concise and measured commu-nication via virtual meetings, will help staff stay focused.

ASCs may react more promptly to pandemic than hospitals due to their lower complexity and confined spaces which enable prompt application of contain-ment measures. During emergency conditions, hospital administrators may consider to reallocate specific pro-cedures such as intravitreal therapies to ASCs in order to limit patients’ access to hospitals, where the risk of being exposed to the infecting agent is higher. We hope that our early experience in enhancing infection control measures in ophthalmology can help physicians to optimally reorganize patient care.

Acknowledgements

This article is dedicated to Dr Li Wenliang and the multitude of physicians and health workers who perished while serving their communities during the COVID-19 pandemic.

Author contributions

provided administrative, technical or material support for this study. F.B. and P.L. supervised this study.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship and/or publication of this article.

ORCID iDs

Francesco Bandello https://orcid.org/0000-0003-3238-9682

Paolo Lanzetta https://orcid.org/0000-0003-3746-141X

References

1. World Health Organization. WHO statement regarding cluster of pneumonia cases in Wuhan, China, www.who. int/china/news/detail/09-01-2020-who-statement-regard ing-cluster-of-pneumonia-cases-in-wuhan-china (2020, accessed 16 March 2020).

2. World Health Organization. Coronavirus disease 2019 (COVID-19) situation report-47, www.who.int/docs/ default-source/coronaviruse/situation-reports/20200307-sitrep-47-covid-19.pdf?sfvrsn=27c364a4_2 (2020, accessed 16 March 2020).

3. Dong E, Du H and Gardner L. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect Dis2020; 20: 533–534.

4. Grasselli G, Pesenti A and Cecconi M. Critical care uti-lization for the COVID-19 outbreak in Lombardy, Italy: early experience and forecast during an emergency response. JAMA. Epub ahead of print 13 March 2020. DOI: 10.1001/jama.2020.4031.

5. Novel Coronavirus Pneumonia Emergency Response Epidemiology Team. The epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (COVID-19) in China. Zhonghua Liu Xing Bing Xue Za Zhi2020; 41: 145–151.

6. Lauer SA, Grantz KH, Bi Q, et al. The incubation period of coronavirus disease 2019 (COVID-19) from publicly reported confirmed cases: estimation and application. Ann Intern Med2020; 172: 577–582.

7. Du Z, Wang L, Cauchemez S, et al. Risk for transporta-tion of coronavirus disease from Wuhan to other cities in China. Emerg Infect Dis 2020; 26: 1049–1052.

8. Xia J, Tong J, Liu M, et al. Evaluation of coronavirus in tears and conjunctival secretions of patients with SARS-CoV-2 infection. J Med Virol 2020; 92: 589–594.

9. Bai Y, Yao L, Wei T, et al. Presumed asymptomatic car-rier transmission of COVID-19. JAMA 2020; 323: 1406–1407.

10. Mizumoto K, Kagaya K, Zarebski A, et al. Estimating the asymptomatic proportion of coronavirus disease 2019

(COVID-19) cases on board the Diamond Princess cruise ship, Yokohama, Japan, 2020. Eurosurveillance 2020; 25: 2000180.

11. Ma J, Lew L and Jeong-ho L. A third of coronavirus cases may be ‘silent carriers’, classified Chinese data sug-gests. South China Morning Post, 22 March 2020, http:// www.scmp.com/news/china/society/article/3076323/th ird-coronavirus-cases-may-be-silent-carriers-classified (accessed 30 March 2020).

12. Petersen E, Hui D, Hamer DH, et al. Li Wenliang, a face to the frontline healthcare worker. The first doctor to notify the emergence of the SARS-CoV-2, (COVID-19), outbreak. Int J Infect Dis 2020; 93: 205–207.

13. Li JPO, Shantha J, Wong TY, et al. Preparedness among ophthalmologists: during and beyond the COVID-19 pandemic. Ophthalmology 2020; 127: 569–572.

14. American Academy of Ophthalmology. Important coro-navirus updates for ophthalmologists, www.aao.org/head line/alert-important-coronavirus-context (2020, accessed 30 March 2020).

15. Royal College of Ophthalmologists. COVID-19 clinical guidance for ophthalmologists, www.rcophth.ac.uk/ 2020/03/covid-19-update-and-resources-for-ophthalmolo gists/ (2020, accessed 30 March 2020).

16. Societa` Oftalmologica Italiana. La societa` oftalmologica italiana indica le azioni per sostenere il diritto di accesso alla cura da parte dei pazienti affetti da patologie oftal-miche, www.soiweb.it/leggi_news.php?id=1883 (2020, accessed 30 March 2020).

17. Associazione Italiana Medici Oculisti. www.oculistiaimo. it/ (2020, accessed 30 March 2020).

18. Kanellopoulos AJ. Protect yourself, staff and patients with a slit-lamp shield!, www.youtube.com/ watch?v=wvnx_KIUE9A (2020, accessed 15 March 2020).

19. Lai THT, Tang EWH, Chau SKY, et al. Stepping up infection control measures in ophthalmology during the novel coronavirus outbreak: an experience from Hong Kong. Graefes Arch Clin Exp Ophthalmol 2020; 258: 1049–1055.

20. Britt JM, Clifton BC, Barnebey HS, et al. Microaerosol formation in noncontact ‘air-puff’ tonometry. Arch Ophthalmol1991; 109: 225–228.

21. Jefferson T, Foxlee R, Del Mar C, et al. Physical interventions to interrupt or reduce the spread of respi-ratory viruses: systematic review. BMJ 2009; 339: b3675. 22. Makison Booth C, Clayton M, Crook B, et al. Effectiveness of surgical masks against influenza bioaer-osols. J Hosp Infect 2013; 84: 22–26.

23. Cowling BJ, Chan KH, Fang VJ, et al. Facemasks and hand hygiene to prevent influenza transmission in house-holds: a cluster randomized trial. Ann Intern Med 2009; 151: 437–446.

25. Istituto Superiore di Sanita`. Sorveglianza integrata COVID-19 in Italia, www.iss.it/documents/20126/0/ Infografica_09marzo.pdf/ (2020, accessed 31 March 2020).

26. European Centre for Disease Prevention and Control. Rapid risk assessment: novel coronavirus disease 2019 (COVID-19) pandemic: increased transmission in the EU/EEA and the UK – sixth update, www.ecdc.europa.

eu/en/publications-data/rapid-risk-assessment-novel-coronavirus-disease-2019-covid-19-pandemic-increased (2020, accessed 30 March 2020).